Signaled two-way avoidance learning using electrical stimulation of the inferior colliculus as negative reinforcement: effects of visual and auditory cues as warning stimuli

Abstract

The inferior colliculus is a primary relay for the processing of auditory information in the brainstem. The inferior colliculus is also part of the so-called brain aversion system as animals learn to switch off the electrical stimulation of this structure. The purpose of the present study was to determine whether associative learning occurs between aversion induced by electrical stimulation of the inferior colliculus and visual and auditory warning stimuli. Rats implanted with electrodes into the central nucleus of the inferior colliculus were placed inside an open-field and thresholds for the escape response to electrical stimulation of the inferior colliculus were determined. The rats were then placed inside a shuttle-box and submitted to a two-way avoidance paradigm. Electrical stimulation of the inferior colliculus at the escape threshold (98.12 ± 6.15 (A, peak-to-peak) was used as negative reinforcement and light or tone as the warning stimulus. Each session consisted of 50 trials and was divided into two segments of 25 trials in order to determine the learning rate of the animals during the sessions. The rats learned to avoid the inferior colliculus stimulation when light was used as the warning stimulus (13.25 ± 0.60 s and 8.63 ± 0.93 s for latencies and 12.5 ± 2.04 and 19.62 ± 1.65 for frequencies in the first and second halves of the sessions, respectively, P<0.01 in both cases). No significant changes in latencies (14.75 ± 1.63 and 12.75 ± 1.44 s) or frequencies of responses (8.75 ± 1.20 and 11.25 ± 1.13) were seen when tone was used as the warning stimulus (P>0.05 in both cases). Taken together, the present results suggest that rats learn to avoid the inferior colliculus stimulation when light is used as the warning stimulus. However, this learning process does not occur when the neutral stimulus used is an acoustic one. Electrical stimulation of the inferior colliculus may disturb the signal transmission of the stimulus to be conditioned from the inferior colliculus to higher brain structures such as amygdala.

Apomorphine Enhances Conditioned Responses Induced by Aversive Stimulation of the Inferior Colliculus

“…The brain stimulation was applied at a current intensity 5% below the escape threshold previously determined in the open field. The adequacy of this current intensity level for the escape response was verified on the basis of a previous study from this laboratory (Melo et al, 1992;Brandão et al, 1997;Troncoso et al, 1998).…”

“…Latent inhibition has been considered as a model for information filtering processesand demonstrates attentional processes in rats that are responsive to drug treatment in a fashion that parallels drug responses seen in humans with schizophrenia (Makintosh, 1975;Lubow et al, 1982;Dunn et al, 1993;Sandner et al, 2002). We have already shown that stimulation of neural circuits in the central nucleus of the IC supports Pavlovian conditioning and that latent inhibition may be demonstrated using stimulation of these neural circuits in the IC as negative reinforcement Troncoso et al, 1998;Castilho and Brandão, 2001).…”

“…The inferior colliculus (IC) is a midbrain tectum structure primarily involved in auditory information processing; it also integrates sensory information of aversive nature. Indeed, electrical or chemical stimulation of this structure induces responses such as freezing and flight responses that mimic fearful behavior elicited by environmental challenges (Schmitt et al, 1986;Brandão et al, 1988Cardoso et al, 1994;Troncoso et al, 1998;Castilho et al, 1999). Several studies have suggested modulatory roles for GABA, serotonin, opioids, excitatory amino acids and neuropeptides at the so-called brain aversion system, which includes the dorsal periaqueductal gray and IC (Brandão et al, 1982.…”

Alterações no processamento da informação sensorial auditiva induzidas pela abstinência ao álcool em ratos: importância dos mecanismos GABAérgicos e glutamatérgicos do colículo inferior

“…Alguns resultados obtidos de experimentos utilizando o paradigma do comportamento operante, no qual os animais se engajam em tarefas que permitem interromper ou desligar a estimulação elétrica do CI (switch-off) nos permitem afirmar a natureza aversiva deste tipo de estímulo, assim como a característica defensiva da resposta (Melo et al, 1992;Brandão et al, 1997 et al, 1980;1993;1994;Melo et al, 1992;Coimbra & Brandão, 1993;Melo & Brandão, 1995b;Maisonnette et al, 1996;Troncoso et al, 1998;Pandóssio & Brandão, 1999;Pandóssio et al, 2000;Cuadra et al, 2000;Castilho & Brandão, 2001;Lamprea et al, 2002;Macedo et al, 2002). A administração local de benzodiazepínicos ou agonistas GABAérgicos (Melo et al, 1992;Pandóssio & Brandão, 1999) e agonistas ou bloqueadores da recaptação de 5-HT (Melo & Brandão, 1995b) aumenta significativamente os limiares aversivos de estimulação elétrica e a latência para a resposta de "switch-off" dessa estimulação.…”

“…Como o CI está primariamente envolvido com o processamento da informação auditiva, isto pode ser importante no processamento da informação acústica de natureza aversiva como, por exemplo, utilizar um som como reforço condicionado negativo (Brandão et al, 1997;Troncoso et al, 1998). Tem sido proposto que neurônios do CI são filtros para sons que precisam de ações imediatas, como certos sons emitidos por presas e predadores (Casseday & Covey, 1996 Brandão et al, 2001;Sandner et al, 2002).…”